What do foraging wasps optimize in a variable ... - Springer Link

J Comp Physiol A (2015) 201:1043–1052 DOI 10.1007/s00359-015-1033-4

ORIGINAL PAPER

What do foraging wasps optimize in a variable environment, energy investment or body temperature? Helmut Kovac1 · Anton Stabentheiner1 · Robert Brodschneider1 

Received: 18 November 2014 / Revised: 28 July 2015 / Accepted: 29 July 2015 / Published online: 19 August 2015 © The Author(s) 2015. This article is published with open access at Springerlink.com

Abstract  Vespine wasps (Vespula sp.) are endowed with a pronounced ability of endothermic heat production. To show how they balance energetics and thermoregulation under variable environmental conditions, we measured the body temperature and respiration of sucrose foragers (1.5 M, unlimited flow) under variable ambient temperature (Ta = 20–35 °C) and solar radiation (20–570 W m−2). Results revealed a graduated balancing of metabolic efforts with thermoregulatory needs. The thoracic temperature in the shade depended on ambient temperature, increasing from ~37 to 39 °C. However, wasps used solar heat gain to regulate their thorax temperature at a rather high level at low Ta (mean Tthorax ~ 39 °C). Only at high Ta they used solar heat to reduce their metabolic rate remarkably. A high body temperature accelerated the suction speed and shortened foraging time. As the costs of foraging strongly depended on duration, the efficiency could be significantly increased with a high body temperature. Heat gain from solar radiation enabled the wasps to enhance foraging efficiency at high ambient temperature (Ta = 30 °C) by up to 63 %. The well-balanced change of economic strategies in response to environmental conditions minimized costs of foraging and optimized energetic efficiency.

Electronic supplementary material  The online version of this article (doi:10.1007/s00359-015-1033-4) contains supplementary material, which is available to authorized users. * Helmut Kovac helmut.kovac@uni‑graz.at Anton Stabentheiner anton.stabentheiner@uni‑graz.at 1



Institute of Zoology, University of Graz, Universitätsplatz 2, 8010 Graz, Austria

Keywords  Energetics · Thermoregulation · Foraging · Wasps · Vespula

Introduction Vespine wasps are heterothermic insects, which are able to switch between an ectothermic and an endothermic state. Their ability of endothermic heat production has been investigated by several authors (e.g. Heinrich 1984; Coelho and Ross 1996; Eckles et al. 2008; Kovac and Stabentheiner 1999, 2012; Kovac et al. 2009). Endothermic heat production by means of the thoracic flight muscles is used for social thermoregulation inside the nest (Steiner 1930; Ishay and Ruttner 1971; Ishay 1973; Klingner et al. 2005, 2006) and also during foraging outside (Eckles et al. 2008; Kovac and Stabentheiner 1999, 2012; Kovac et al. 2009). Foraging vespine wasps are often highly endothermic because their flight muscles must achieve a minimum threshold temperature for proper take off and flight (e.g. Heinrich 1984, 1993; Coelho and Ross 1996; Kovac and Stabentheiner 2012). They can reach thoracic temperatures higher than 40 °C (Heinrich 1984; Kovac and Stabentheiner 1999; Kovac et al. 2009). In water-collecting honeybees, a high thorax temperature enables bees to elevate the temperature of the head to a rather high level and increase suction speed (Kovac et al. 2010). On the other hand, endothermy and a high body temperature mean also high costs. Foraging strategies of social insects balance energy expenditure of individual foragers with the net energetic gains to the colony (e.g. Seeley 1986; Seeley et al. 1991; Varjú and Núñez 1991). During foraging, vespine wasps are exposed to highly variable environmental conditions. In a temperate climate, ambient temperature may range from 2 to 38 °C (Heinrich 1984,

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1993; Kovac and Stabentheiner 1999, 2012; Kovac et al. 2009). Solar radiation may vary from 20 to 1200 W m−2 (Kovac et al. 2009; Kovac and Stabentheiner 2012). However, variation in ambient air temperature can greatly affect the energy expended by foragers. Thus, some wasps and bees alter their metabolic or thermoregulatory activity rates to respond to changes in ambient temperature (Heinrich 1993; Schmolz et al. 1999). Besides ambient air temperature, the influence of solar radiation on insect thermoregulation is not negligible. Its effect on the body temperature of water foraging vespine wasps (Vespula sp.) has been investigated by Kovac et al. (2009). The body temperature was positively correlated with solar radiation, and the thoracic temperature excess was more pronounced at moderate (Ta = 22–28 °C) than at high ambient temperatures (>30 °C). At high Ta, the wasps reduced active thermoregulation but kept nevertheless a high body temperature. For a comprehensive assessment of energetic optimization strategies of foraging insects, it is of great advantage to measure both thermoregulatory behaviour and metabolic rate (Stabentheiner et al. 2012). In honeybee foragers, this allowed new insights into the adaptation of economic strategies to variations of environmental conditions (Stabentheiner et al. 2012; Stabentheiner and Kovac 2014). However, in vespine wasps no investigations on foraging energetics are available. The aim of this study was to combine both body temperature measurement with respiration measurement (CO2 production) to assess energetic and thermoregulatory optimization strategies of foraging wasps under field conditions. In detail, we investigated what the foragers actually optimize: Do they use heat gain from solar radiation to elevate their body temperature or for the minimization of their energetic expenditure? Do they optimize energetic efficiency or foraging time, or both? The investigations should enable us to differentiate how wasps adapt their energetic strategy during foraging to different environmental challenges.

Materials and methods Location and experimental setup Experiments were conducted in September and October 2006 in Gschwendt, in a garden close to an external laboratory facility of the University of Graz, Austria. To measure body temperature, respiration and load weight, ten wasps (Vespula germanica) were marked individually with colour dots on thorax and abdomen. They were trained to collect 1.5 molar sucrose solutions in a respiratory measurement chamber (Fig. 1; ~7.9 ml inner volume)

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J Comp Physiol A (2015) 201:1043–1052

Fig.  1  a Thermogram of a wasp foraging sucrose solution from an artificial flower inside a respiratory measurement chamber. Air inlet is at the bottom of the image, outlet is in the chamber floor right to the wasp. The thorax is heated by activation of the flight muscles, part of the heat has reached the head and the abdomen. Ta ~ 22 °C. Right-hand rectangle proprietary infrared reference radiator. b Wasp foraging sucrose solution from an artificial flower inside a respiratory measurement chamber. On the left side, the global radiation sensor for measuring the solar radiation is visible

endowed with an artificial flower. The artificial flower was constructed from a cap of a plastic vial as described in Stabentheiner et al. (2012) and Stabentheiner and Kovac (2014). The sucrose solution was offered in this plastic vial where the wasps could suck it. Sucrose solution was delivered unlimitedly to the artificial flower by a perfusor (B-BRAUN Perfusor Compact). To get access to the measurement chamber, the wasps had to pass through a balance (AB104, METTLER-TOLEDO, Greifensee, Switzerland), where they were weighed before and after foraging to measure their load weight. Leaving the balance they had to enter the measurement chamber via a short tunnel. Immediately after entering the chamber, the chamber lid was closed and after finishing sucking the lid was opened manually. During experiments, the chamber was kept closed air tight.

J Comp Physiol A (2015) 201:1043–1052

Ambient temperature and solar radiation in chamber Body surface temperature and CO2 production of each individual were measured during 5–10 foraging bouts at the same environmental condition. The variable environmental conditions were ambient air temperature and solar radiation. Experimental ambient temperature in the brass respiratory measurement chamber, which was immersed in a water bath (Julabo F33 HT) for temperature control, was regulated from 20 to 35 °C. If possible, the same wasp was measured both in bright sunshine and artificial shadowing at the same experimental ambient temperature. Sometimes wasps were foraging at intermediate, cloudy conditions. These measurements were also evaluated and taken into consideration. Ambient air temperature was measured about 1 cm beside the wasps in the measurement chamber by a Type K thermocouple. Solar radiation was measured using a custom-manufactured photoelectric miniature global radiation sensor (FLA613GS/Mini spezial, measurement range of 380–1100 nm; Ahlborn) in a second chamber beside that containing the artificial flower (Stabentheiner et al. 2012; Stabentheiner and Kovac 2014). Air temperature in the measurement chamber, radiation and outside air temperature were recorded with an ALMEMO® data logger (28909; Ahlborn). Results were divided into three categories according to the mean solar radiation during the foraging stay, bright sunshine (>500 W m−2, mean = 533 W m−2), partial sunshine (100–500 W m−2, mean = 398 W m−2) and shade (